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Neurobiology of spatial memory
Physiology Hippocampus The hippocampus provides animals with a spatial map of their environment.O’Keefe, J. & Dostrovsky, J. (1971). The hippocampus as a spatial map. Preliminary evidence from unit activity in the freely-moving rat. Brain Research, 34, 171-175. It stores information regarding non-egocentric space (egocentric means in reference to one's body position in space) and therefore supports viewpoint independence in spatial memory.Squire, L. R. (1992). Memory and the hippocampus: A synthesis from findings with rats, monkeys, and humans. Psychological Review, 99(2), 195-231. This means that it allows for viewpoint manipulation from memory. It is however, important for long-term spatial memory of allocentric space (reference to external cues in space).Ramos, J. M. J. (2000). Long-term spatial memory in rats with hippocampal lesions. European Journal of Neuroscience, 12, 3375-3384. Maintenance and retrieval of memories are thus relational or context dependent.Winocur, G., Moscovitch, M., Caruana, D. A. & Binns, M. A. (2005). Retrograde amnesia in rats with lesions to the hippocampus on a test of spatial memory. Neuropsychologia, 43, 1580-1590. The hippocampus makes use of reference and working memory and has the important role of processing information about spatial locations. Blocking plasticity in this region results in problems in goal-directed navigation and impairs the ability to remember precise locations.Hebert, A. E. & Dash, P. K. (2004). Nonredundant roles for hippocampal and entorhinal cortical plasticity in spatial memory storage. Pharmacology, Biochemistry and Behavior, 79, 143-153. Amnesic patients with damage to the hippocampus cannot learn or remember spatial layouts and patients having undergone hippocampal removal are severely impaired in spatial navigation.Morris, R. G. M., Garrud, P., Rawlins, J. N. P. & O’Keefe, J. (1982). Place navigation impaired in rats with hippocampal lesions. Natrue, 297, 681-683. Monkeys with leisons to this area cannot not learn object-place associations and rats also display spatial deficits by not reacting to spatial change.Save, E., Poucet, B., Foreman, N. & Buhot, M. (1992). Object exploration and reactions to spatial and nonspatial changes in hooded rats following damage to parietal cortex or hippocampal formation. Behavioral Neuroscience, 106(3), 447-456. In addition, rats with hippocampal lesions were shown to have temporally ungraded (time-independent) retrograde amnesia that is only resistant to recognition of a learned platform task when the entire hippocampus is lesioned but not when it is partially lesioned.Martin, S. J., de Hozl, L. & Morris, R. G. M. (2005). Retrograde amnesia: neither partial nor complete hippocampal lesions in rats result in preferential sparing of remote spatial memory, even after reminding. Neuropsychologia, 43, 609-624. Deficits in spatial memory are also found in spatial discrimination tasks. Large differences in spatial impairment are found among the dorsal and ventral hippocampus. Lesions to the ventral hippocampus have no effect on spatial memory, while the dorsal hippocampus is required for retrieval, processing short-term memory and transferring memory from the short term to longer delay periods.Bannerman, D. M., Deacon, R. M. J., Offen, S., Friswell, J., Grubb, M. & Rawlins, J. N. P. (2002). Double dissociation of function within the hippocampus: Spatial memory and hyponeophagia. Behavioral Neuroscience, 116(5), 884-901.Moser, M. & Moser, E. I. (1998). Distributed encoding and retrieval of spatial memory in the hippocampus. The Journal of Neuroscience, 18(18), 7535-7542.Lee, I. & Kesner, R. P. (2003). Time-dependent relationship between the dorsal hippocampus and the prefrontal cortex in spatial memory. The Journal of Neuroscience, 23(4), 1517-1523. Infusion of amphetamine into the dorsal hippocampus has also been shown to enhance memory for spatial locations learned previously.McGaugh, J. L. (2000). Memory—a century of consolidation. Science, 287, 248-251. These findings indicate that there is a functional dissociation between the dorsal and ventral hippocampus. Hemispheric differences within the hippocampus are also observed. A study on London taxi drivers, asked drivers to recall complex routes around the city as well as famous landmarks for which the drivers had no knowledge of their spatial location. This resulted in an activation of the right hippocampus solely during recall of the complex routes which indicates that the right hippocampus is used for navigation in large scale spatial environments.Maguire, E. A., Frackowiak, R. S. J. & Frith, C. D. (1997). Recalling routes around London: Activation of the right hippocampus in taxi drivers. The Journal of Neuroscience, 17(18), 7103-7110. The hippocampus is known to contain two separate memory circuits. One circuit is used for recollection-based place recognition memory and includes the entorhinal-CA1 system while the other system is used for place recall memory and makes use of the CA3-CA1 system.Brun, V. H., Otnaess, M. K., Molden, S., Steffenach, H., Witter, M. P., Moser, M. & Moser, E. I. (2002). Place cells and place recognition maintained by direct entorhinal-hippocampal circuitry. Science, 296, 2243-2246. Place cells are also found in the hippocampus. Posterior parietal cortex The parietal cortex encodes spatial information using an egocentric frame of reference. It is therefore involved in the transformation of sensory information coordinates into action or effector coordinates by updating the spatial representation of the body within the environment.Colby, C. L. & Goldberg, M. E. (1999). Space and attention in parietal cortex. Annual Review of Neuroscience, 22, 319-349. As a result, lesions to the parietal cortex produce deficits in the acquisition and retention of egocentric tasks, whereas minor impairment is seen among allocentric tasks.Save, E. & Moghaddam, M. (1996). Effects of lesions of the associative parietal cortex on the acquisition and use of spatial memory in egocentric and allocentric navigation tasks in the rat. Behavioral Neuroscience, 110(1), 74-85. Rats with lesions to the anterior region of the posterior parietal cortex reexplore displaced objects, while rats with lesions to the posterior region of the posterior parietal cortex displayed no reaction to spatial change. Parietal cortex lesions are also known to produce temporally ungraded retrograde amnesia.Cho, Y. H. & Kesner, R. P. (1996). Involvement of entorhinal cortex or parietal cortex in long-term spatial discrimination memory in rats: Retrograde amnesia. Behavioral Neuroscience, 110(3), 436-442. Entorhinal cortex The dorsalcaudal medial entorhinal cortex (dMEC) contains a topographically organized map of the spatial environment made up of grid cells.Hafting, T., Fyhn, M., Molden, S., Moser, M. & Moser, E. I. (2005). Microstructure of a spatial map in the entorhinal cortex. Nature, 436, 801-806. This brain region thus transforms sensory input from the environment and stores it as a durable allocentric representation in the brain to be used for path integration.Fyhn, M., Molden, S., Witter, M. P., Moser, E. I. & Moser, M. (2004). Spatial representation in the entorhinal cortex. Science, 305, 1258-1264. The entorhinal cortex contributes to the processing and integration of geometric properties and information in the environment.Parron, C. & Save, E. (2004). Comparison of the effects of entorhinal and retrosplenial cortical lesions on habituation, reaction to spatial and non-spatial changes during object exploration in the rat. Neurobiology of Memory and Learning, 82, 1-11. Lesions to this region impair the use of distal but not proximal landmarks during navigation and produces a delay-dependent deficit in spatial memory that is proportional to the length of the delay.Parron, C., Poucet, B. & Save, E. (2004). Entorhinal cortex lesions impair the use of distal but not proximal landmarks during place navigation in the rat. Behavioural Brain Research, 154, 345-352.Nagahara, H. A., Otto, T. & Gallagher, M. (1995). Entorhinal-perirhinal lesions impair performance of rats on two versions of place learning in the Morris water maze. Behavioral Neuroscience, 109(1), 3-9. Lesions to this region are also known to create retention deficits for tasks learned up to 4 weeks but not 6 weeks prior to the lesions. Memory consolidation in the entorhinal cortex is achieved through extracellular signal-regulated kinase activity.Hebert, A. E. & Dash, P. K. (2002). Extracellular signal-regulated kinase activity in the entorhinal cortex is necessary for long-term spatial memory. Learning & Memory, 9, 156-166. Prefrontal cortex The medial prefrontal cortex processes egocentric spatial information. It participates in the processing of short-term spatial memory used to guide planned search behavior and is believed to join spatial information with its motivational significance.Pratt, W. E. & Mizumori, S. J. Y. (2001). Neurons in rat medial prefrontal cortex show anticipatory rate changes to predictable differential rewards in a spatial memory task. Behavioural Brain Research, 123, 165-183. The identification of neurons that anticipate expected rewards in a spatial task support this hypothesis. The medial prefrontal cortex is also implicated in the temporal organization of information.Kesner, R. P. & Holbrook, T. (1987). Dissociation of item and order spatial memory in rats following medial prefrontal cortex lesions. Neuropsychologia, 25(4), 653-664. Hemisphere specialization is found in this brain region. The left prefrontal cortex preferentially processes categorical spatial memory including source memory (reference to spatial relationships between a place or event), while the right prefrontal cortex preferentially processes coordinate spatial memory including item memory (reference to spatial relationships between features of an item).Slotnick, S. D. & Moo, L. R. (2006). Prefrontal cortex hemispheric specialization for categorical and coordinate visual spatial memory. Neuropsychologia, 44, 1560-1568. Leisons to the medial prefrontal cortex impair the performance of rats on a previously trained radial arm maze, however, rats can gradually improve to the level of the controls as a function of experience.Becker, J. T., Walker, J. A. & Olton, D. S. (1980). Neuroanatomical bases of spatial memory. Brain Research, 200, 307-320. Lesions to this area also cause deficits on delayed nonmatching-to-positions tasks and impairments in the acquisition of spatial memory tasks during training trials.Aggleton, J. P., Neave, N., Nagle, S. & Sahgal, A. (1995). A comparison of the effects of medial prefrontal, cingulate cortex, and cingulum bundle lesions on tests of spatial memory: Evidence of a double dissociation between frontal and cingulum bundle contributions. The Journal of Neuroscience, 15(11), 7270-7281.Lacroix, L., White, I. & Feldon, J. (2002). Effect of excitotoxic lesions of rat medial prefrontal cortex on spatial memory. Behavioural Brain Research, 133, 69-81. Retrosplenial cortex The retrosplenial cortex is involved in the processing of allocentric memory and geometric properties in the environment. Inactivation of this region accounts for impaired navigation in the dark and thus it is implicated to be involved in the process of path integration.Cooper, B. G., Manka, T. F. & Mizumori, S. J. Y. (2001). Finding your way in the dark: The retrosplenial cortex contributes to spatial memory and navigation without visual cues. Behavioral Neuroscience, 115(5), 1012-1028. Lesions to the retrosplenial cortex consistently impair tests of allocentric memory, while sparing egocentric memory.Vann, S. D. & Aggleton, J. P. (2002). Extensive cytotoxic lesions of the rat retrosplenial cortex reveal consistent deficits on tasks that tax allocentric spatial memory. Behavioral Neuroscience, 116(1), 85-94. Animals with lesions to the caudal retrosplenial cortex show impaired performance on a radial arm maze only when the maze is rotated to remove their reliance on intramaze cues.Vann, S. D., Wilton, L. A., Muir, J. L. & Aggleton, J. P. (2003). Testing the importance of the caudal retrosplenial cortex for spatial memory in rats. Behavioural Brain Research, 140, 107-118. In humans, damage to the retrosplenial cortex results in topographical disorientation. Most cases involve damage to the right retrosplenial cortex and include Broadmann’s area 30. Patients are often impaired at learning new routes and at navigating through familiar environments.Maguire, E. A. (2001). The retrosplenial contribution to human navigation: A review of lesion and neuroimaging findings. Scandinavian Journal of Psychology, 42, 225-238. However, most patients usually recover within 8 weeks. The retrosplenial cortex preferentially processes spatial information in the right hemisphere. Perirhinal cortex The perirhinal cortex is associated with both spatial reference and spatial working memory.Liu, P. & Bilkey, D. K. (2001). The effect of excitotoxic lesions centered on the hippocampus or perirhinal cortex in object recognition and spatial memory tasks. Behavioral Neuroscience, 115(1), 94-111. It processes relational information of environmental cues and locations. Lesions in the perirhinal cortex account for deficits in reference memory and working memory, and increase the rate of forgetting of information during training trials of the Morris water maze.Liu, P. & Bilkey, D. K. (1998). Perirhinal cortex contributions to performance in the Morris water maze. Behavioral Neuroscience, 112(2), 304-315. This accounts for the impairment in the initial acquisition of the task. Lesions also cause impairment on an object location task and reduce habituation to a novel environment. Plasticity Spatial memories are formed after an animal gathers and processes sensory information about its surroundings (especially vision and proprioception). In general, mammals require a functioning hippocampus (particularly area CA1) in order to form and process memories about space. There is some evidence that human spatial memory is strongly tied to the right hemisphere of the brain.Gutbrod K, Cohen R, Maier T, Meier E (September 1987). "Memory for spatial and temporal order in aphasics and right hemisphere damaged patients". Cortex 23 (3): 463–74.Nunn JA, Graydon FJ, Polkey CE, Morris RG (January 1999). "Differential spatial memory impairment after right temporal lobectomy demonstrated using temporal titration". Brain 122 (Pt 1): 47–59.Tucker DM, Hartry-Speiser A, McDougal L, Luu P, deGrandpre D (June 1999). "Mood and spatial memory: emotion and right hemisphere contribution to spatial cognition". Biol Psychol 50 (2): 103–25. Spatial learning requires both NMDA and AMPA receptors, consolidation requires NMDA receptors, and the retrieval of spatial memories requires AMPA receptors.Liang KC, Hon W, Tyan YM, Liao WL (1994). "Involvement of hippocampal NMDA and AMPA receptors in acquisition, formation and retrieval of spatial memory in the Morris water maze". Chin J Physiol 37 (4): 201–12. In rodents, spatial memory has been shown to covary with the size of a part of the hippocampal mossy fiber projection.W. E. Crusio & H. Schwegler (2005). "Learning spatial orientation tasks in the radial-maze and structural variation in the hippocampus in inbred mice". Behavioral and Brain Functions 1 (1): 3. The function of NMDA receptors varies according to the subregion of the hippocampus. NMDA receptors are required in the CA3 of the hippocampus when spatial information needs to be reorganized, while NMDA receptors in the CA1 are required in the acquisition and retrieval of memory after a delay, as well as in the formation of CA1 place fields.Lee, I. & Kesner, R. P. (2002). Differential contribution of NMDA receptors in hippocampal subregions to spatial working memory. Nature Neuroscience, 5(2), 162-168. Blockade of the NMDA receptors prevents induction of long-term potentiation and impairs spatial learning.Morris, R. G. M., Anderson, E., Lynch, G. S. & Baudry, M. (1986). Selective impairment of learning and blockade of long-term potentiation by an N-methyl-D-aspartate receptor anatagonist, AP5. Nature, 319, 774-776. The CA3 of the hippocampus plays an especially important role in the encoding and retrieval of spatial memories. The CA3 is innervated by two afferent paths known as the perforant path (PPCA3) and the dentate gyrus (DG)-mediated mossy fibers (MFs). The first path is regarded as the retrieval index path while the second is concerned with encoding.Lee, I. & Kesner, R. P. (2004). Encoding versus retrieval of spatial memory: Double dissociation between the dentate gyrus and the perforant path inputs into CA3 in the dorsal hippocampus. Hippocampus, 14, 66-76. References